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Population Genetic Structure and Conservation of the Galápagos Petrel (Pterodroma phaeopygia)

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Abstract

The Galápagos petrel (Pterodroma phaeopygia) is endemic to the Galápagos archipelago, where it is known to breed only on five islands. The species has been listed as critically endangered due to habitat deterioration and predation by introduced mammals. Significant morphological and behavioural differences among petrels nesting on different islands suggest that island populations may differ genetically. Furthermore, nesting phenology suggests that genetically differentiated seasonal populations may exist within at least one island. We analysed variation in six microsatellite loci and part of the mitochondrial ATPase 6/8 gene in 206 Galápagos petrels sampled from all five islands. No evidence of genetic structuring within islands was found, although statistical power was low. In contrast, significant differences occurred among island populations. For the microsatellite loci, private alleles occurred at all islands, sometimes at high frequency; global and pairwise estimates of genetic differentiation were all statistically significant; Bayesian analysis of genotypes frequencies provided strong support for three genetic populations; and most estimates of migration between populations did not differ significantly from zero. Only two ATPase haplotypes were found, but the geographic distribution of haplotypes indicated significant differentiation among populations. For conservation purposes, populations from Floreana, Santa Cruz, San Cristóbal and Santiago should be regarded as separate genetic management units. Birds from Isabela appear to be derived recently from the Santiago population, and the population on San Cristóbal appears to be a mixture of birds from other populations. However, considering ecological and behavioural differences among birds from different islands, we recommend that all five populations be protected.

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References

  • CL Abbott MC Double (2003) ArticleTitleGenetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses Mol. Ecol. 12 2953–2963 Occurrence Handle14629376

    PubMed  Google Scholar 

  • D Ainley (1980) ArticleTitleGeographic variation in Leach’s Storm-petrel Auk 97 937–853

    Google Scholar 

  • P Beerli (1999) Estimation of migration rates and population sizes in geographically structured populations G Carvalho (Eds) Advances in Molecular Ecology NATO-ASI Workshop Series ISO, Amsterdam

    Google Scholar 

  • LB Beheregaray JP Gibbs N Havill et al. (2004) ArticleTitleGiant tortoises are not so slow: rapid diversification and biogeographic consensus in the Galapagos Proc. Natl. Acad. Sci. USA 101 6514–6519 Occurrence Handle10.1073/pnas.0400393101 Occurrence Handle1:CAS:528:DC%2BD2cXjvVyitbo%3D Occurrence Handle15084743

    Article  CAS  PubMed  Google Scholar 

  • RA Browne DJ Anderson JN Houser F Cruz KJ Glasgow CN Hodges G Massey (1997) ArticleTitleGenetic diversity and divergence of endangered Galápagos and Hawaiian petrel populations Condor 99 812–815

    Google Scholar 

  • TM Burg (1999) ArticleTitleIsolation and characterization of microsatellites in albatrosses Mol. Ecol. 8 338–341 Occurrence Handle1:CAS:528:DyaK1MXjtVOnsrw%3D Occurrence Handle10065551

    CAS  PubMed  Google Scholar 

  • TM Burg JP Croxall (2001) ArticleTitleGlobal relationships amongst black-browed and grey-headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites Mol. Ecol. 10 2647–2660 Occurrence Handle10.1046/j.0962-1083.2001.01392.x Occurrence Handle1:CAS:528:DC%2BD3MXpt12ls7Y%3D Occurrence Handle11883879

    Article  CAS  PubMed  Google Scholar 

  • TM Burg JP Croxall (2004) ArticleTitleGlobal population structure and taxonomy of the wandering albatross species complex Mol. Ecol. 13 2345–2355 Occurrence Handle10.1111/j.1365-294X.2004.02232.x Occurrence Handle1:CAS:528:DC%2BD2cXmsl2rurc%3D Occurrence Handle15245406

    Article  CAS  PubMed  Google Scholar 

  • Byers JA (1999) Earth: great circle distance calculator. Available at http://www.wcrl.ars.usda.gov/cec.java.lat-long.htm.

  • CDF-WWF (2002) A biodiversity vision for the Galápagos Islands. In: Charles Darwin Foundation and World Wildlife Fund (ed. Bensted-Smith R), Puerto Ayora, Galápagos.

  • LL Cavalli-Sforza AWF Edwards (1967) ArticleTitlePhylogenetic analysis: models and estimation procedures Am. J. Hum. Gen. 19 233–257

    Google Scholar 

  • C Ciofi MC Milinkovitch JP Gibbs A Caccone JR Powell (2002) ArticleTitleMicrosatellite analysis of genetic divergence among populations of giant Galapagos tortoises Mol. Ecol. 11 2265–2283 Occurrence Handle10.1046/j.1365-294X.2002.01617.x Occurrence Handle1:CAS:528:DC%2BD38XptlSmu7k%3D Occurrence Handle12406238

    Article  CAS  PubMed  Google Scholar 

  • BC Congdon JF Piatt K Martin VL Friesen (2000) ArticleTitleRapid population expansion and peripheral isolation in marbled murrelets: historical vs. contemporary evolutionary processes Evolution 54 974–986 Occurrence Handle1:STN:280:DC%2BD3cvhvFyhug%3D%3D Occurrence Handle10937270

    CAS  PubMed  Google Scholar 

  • MC Coulter (1984) ArticleTitleSeabird conservation in the Galápagos Islands, Ecuador ICBP Tech. Publ. 2 237–244

    Google Scholar 

  • MC Coulter F Cruz J Cruz (1985) ArticleTitleA programme to save the dark-rumped petrel, Pterodroma phaeopygia, on Floreana Island, Galápagos, Ecuador ICBP Tech. Publ. 3 177–180

    Google Scholar 

  • KA Crandall ORP Bininda-Emonds GM Mace RK Wayne (2000) ArticleTitleConsidering evolutionary processes in conservation biology Trends Ecol. Evol. 5 290–295

    Google Scholar 

  • F Cruz JB Cruz (1990) ArticleTitleBreeding, morphology, and growth of the endangered dark-rumped petrel Auk 107 317–326

    Google Scholar 

  • JB Cruz F Cruz (1987) ArticleTitleConservation of the dark-rumped petrel Pterodroma phaeopygia in the Galápagos Islands, Ecuador Biol. Conserv. 42 303–311 Occurrence Handle10.1016/0006-3207(87)90074-7

    Article  Google Scholar 

  • P-yA Crochet JZ Chen J-M Pons J-D Lebreton PD Hebert F Bonhomme (2003) ArticleTitleGenetic differentiation at nuclear and mitochondrial loci among large white-headed gulls: sex-biased interspecific gene flow? Evolution 57 2865–2878 Occurrence Handle1:CAS:528:DC%2BD2cXhtV2nsLg%3D Occurrence Handle14761064

    CAS  PubMed  Google Scholar 

  • RJG Dawson HL Gibbs KA Hobson SM Yezerinac (1997) ArticleTitleIsolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies Heredity 79 506–514 Occurrence Handle10.1038/sj.hdy.6882050 Occurrence Handle1:CAS:528:DyaK2sXnsFagur8%3D Occurrence Handle9369012

    Article  CAS  PubMed  Google Scholar 

  • L Excoffier PE Smouse JM Quattro (1992) ArticleTitleAnalysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data Genetics 131 479–491 Occurrence Handle1:CAS:528:DyaK38XlsVCntro%3D Occurrence Handle1644282

    CAS  PubMed  Google Scholar 

  • D Falush M Stephens JK Pritchard (2003) ArticleTitleInference of population structure using multilocus genotype data: linked loci and correlated allele frequencies Genetics 164 1567–1587 Occurrence Handle1:CAS:528:DC%2BD3sXnvF2ntrk%3D Occurrence Handle12930761

    CAS  PubMed  Google Scholar 

  • JR Freeland PT Boag (1999) ArticleTitlePhylogenetics of Darwin’s finches: paraphyly in the tree-finches, and two divergent lineages in the warbler finch Auk 116 577–588

    Google Scholar 

  • VL Friesen BC Congdon HE Walsh TP Birt (1997) ArticleTitleIntron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms Mol. Ecol. 6 1047–1058 Occurrence Handle10.1046/j.1365-294X.1997.00277.x Occurrence Handle1:CAS:528:DyaK2sXnslyktLY%3D Occurrence Handle9394463

    Article  CAS  PubMed  Google Scholar 

  • OE Gaggiotti O Lange K Rassmann C Gliddon (1999) ArticleTitleA comparison of two indirect methods for estimating average levels of gene flow using microsatellite data Mol. Ecol. 8 1513–1520 Occurrence Handle10.1046/j.1365-294x.1999.00730.x Occurrence Handle1:CAS:528:DyaK1MXntlakur0%3D Occurrence Handle10564457

    Article  CAS  PubMed  Google Scholar 

  • M Genovart D Oro F Bonhomme (2003) ArticleTitleGenetic and morphological differentiation between the two largest breeding colonies of Audouin’s gull Larus audouinii Ibis 145 448–456 Occurrence Handle10.1046/j.1474-919X.2003.00187.x

    Article  Google Scholar 

  • AD Given JA Mills AJ Baker (2002) ArticleTitleIsolation of polymorphic microsatellite loci from the red-billed gill (Larus novaehollandiae scopulinus) and amplification in related species Mol. Ecol. Notes 2 416–418 Occurrence Handle10.1046/j.1471-8286.2002.00261.x Occurrence Handle1:CAS:528:DC%2BD38XpvVSjtrk%3D

    Article  CAS  Google Scholar 

  • A Goostrey DN Carss LR Noble SB Piertney (1998) ArticleTitlePopulation introgression and differentiation in the great cormorant Phalacrocorax carbo in Europe Mol. Ecol. 7 329–338 Occurrence Handle10.1046/j.1365-294X.1998.00361.x

    Article  Google Scholar 

  • S Guo E Thomson (1992) ArticleTitlePerforming the exact test of Hardy–Weinberg proportion for multiple alleles Biometrics 48 361–372 Occurrence Handle1:STN:280:By2A2crltlY%3D Occurrence Handle1637966

    CAS  PubMed  Google Scholar 

  • MP Harris (1970) ArticleTitleThe biology of an endangered species, the Dark-rumped Petrel (Pterodroma phaeopygia), in the Galápagos Islands Condor 72 76–84

    Google Scholar 

  • K Hayashi (1991) ArticleTitlePCR-SSCP: a simple and sensitive method for detection of mutations in the genomic DNA PCR Meth. Applic. 1 34–38 Occurrence Handle1:CAS:528:DyaK38XhsVCrtrc%3D

    CAS  Google Scholar 

  • PW Hedrick (1999) ArticleTitleHighly variable loci and their interpretation in evolution and conservation Evolution 53 313–318

    Google Scholar 

  • Hilton-Taylor C (2000) The 2000 IUCN Red List of threatened species. IUCN, Gland, Switzerland, and Cambridge, UK.

  • Jiménez G, Wiedenfeld DA (2002) Aves marinas. In: Reserva Marina de Galápagos. Línea Base de la Biodiversidad (eds. Danulat E, Edgar GH), pp. 343–372. Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Puerto Ayora, Galápagos.

  • M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences J. Mol. Evol. 16 111–120 Occurrence Handle10.1007/BF01731581 Occurrence Handle1:CAS:528:DyaL3MXmtFSktg%3D%3D Occurrence Handle7463489

    Article  CAS  PubMed  Google Scholar 

  • D Lack (1966) Population Studies of Birds Clarendon Press Oxford

    Google Scholar 

  • Langella O (2002) Populations 1.2.28. Population Genetic Software (Individuals or Populations Distances, Phylogenetic Trees). Available from http://www.cnrs-gif.fr/pge/bioinfo/populations/index.php.

  • S Manel OE Gaggiotti RS Waples (2005) ArticleTitleAssignment methods: matching biological questions with appropriate techniques Trends Ecol. Evol. 20 136–142 Occurrence Handle10.1016/j.tree.2004.12.004

    Article  Google Scholar 

  • LR Monteiro RW Furness (1998) ArticleTitleSpeciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? Phil. Trans. R. Soc. Lond. B 353 945–953 Occurrence Handle10.1098/rstb.1998.0259

    Article  Google Scholar 

  • C Moritz (1994) ArticleTitleDefining “evolutionary significant units” for conservation Trends Ecol. Evol. 9 373–375

    Google Scholar 

  • M Nei (1987) Molecular Evolutionary Genetics Columbia University Press New York.

    Google Scholar 

  • GB Nunn DJ Anderson (1999) ArticleTitlePhylogenetic relationships among Pacific Pterodroma petrels Proc. Am. Assoc. Advanc. Sci., Pacif. Div. 18 72

    Google Scholar 

  • K Petren BR Grant PR Grant (1999) ArticleTitleA phylogeny of Darwin’s finches based on microsatellite DNA length variation Proc. Roy. Soc. Lond. B 266 321–329 Occurrence Handle1:CAS:528:DyaK1MXhvFWhsL0%3D

    CAS  Google Scholar 

  • J-M Pons P-A Crochet M Thery A Bermejo (2004) ArticleTitleGeographical variation in the yellow-legged gull: introgression or convergence from the herring gull? J. Zool. Syst. Evol. Res. 42 245–256

    Google Scholar 

  • JK Pritchard M Stephens P Donnelly (2000) ArticleTitleInference of population structure using multilocus genotype data Genetics 155 945–959 Occurrence Handle1:STN:280:DC%2BD3cvislKrtA%3D%3D Occurrence Handle10835412

    CAS  PubMed  Google Scholar 

  • Pritchard JK, Wen W (2003) Documentation for Structure Software: Version 2. http://pritch.bsd.uchicago.edu.

  • K Rassmann D Tautz F Trillmich C Gliddon (1997) ArticleTitleThe microevolution of the Galapagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses Mol. Ecol. 6 437–452 Occurrence Handle10.1046/j.1365-294X.1997.00209.x Occurrence Handle1:CAS:528:DyaK2sXjsFOjsLk%3D

    Article  CAS  Google Scholar 

  • DH Reed R Frankham (2003) ArticleTitleCorrelation between fitness and genetic diversity Cons. Biol. 17 230–237

    Google Scholar 

  • WR Rice (1989) ArticleTitleAnalyzing tables of statistical tests Evolution 43 223–225

    Google Scholar 

  • L Riffault KD McCoy C Tirard VL Friesen T Boulinier (2005) ArticleTitlePopulation genetics of the common guillemot Uria aalge in␣the North Atlantic: assessing the geographic impact of oil spills Mar. Ecol. Progr. Ser. 291 263–273

    Google Scholar 

  • AD Roeder KM Richelle AJ Mitchelson et al. (2001) ArticleTitleGene flow on the ice: genetic differentiation among Adélie penguin colonies around Antarctica Mol. Ecol. 10 1645–1656 Occurrence Handle10.1046/j.0962-1083.2001.01312.x Occurrence Handle1:CAS:528:DC%2BD3MXlvVynsrY%3D Occurrence Handle11472533

    Article  CAS  PubMed  Google Scholar 

  • N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: a new method for reconstructing phylogenetic trees Mol. Biol. Evol. 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  • S Schneider JM Kueffer D Roessli L Excoffier (1997) ARLEQUIN ver. 1.1: A Software for Population Genetic Analysis Genetics and Biometry Laboratory, University of Geneva Switzerland

    Google Scholar 

  • G Seutin BN White PT Boag (1991) ArticleTitlePreservation of avian blood and tissue samples for DNA analyses Can. J. Zool. 69 82–90 Occurrence Handle1:CAS:528:DyaK3MXlslylur4%3D

    CAS  Google Scholar 

  • CG Sibley BL Monroe SuffixJr. (1993) Distribution and Taxonomy of Birds of the World-supplement Yale University Press New Haven, CT

    Google Scholar 

  • M Slatkin (1995) ArticleTitleA measure of population subdivision based on microsatellite allele frequencies Genetics 139 457–462 Occurrence Handle1:STN:280:ByqB38%2FmvVE%3D Occurrence Handle7705646

    CAS  PubMed  Google Scholar 

  • M Slatkin L Excoffier (1996) ArticleTitleTesting for linkage disequilibrium in genotypic data using the EM algorithm Heredity 76 377–383 Occurrence Handle8626222

    PubMed  Google Scholar 

  • PE Smouse JC Long RR Sokal (1986) ArticleTitleMultiple regression and correlation extensions of the Mantel Test of matrix correspondence Syst. Zool. 35 627–632

    Google Scholar 

  • HF Stanley S Casey JM Carnahan S Goodman J Harwood RK Wayne (1992) ArticleTitleWorldwide patterns of mitochondrial DNA differentiation in the harbour seal (Phoca vitulina) Mol. Biol. Evol. 13 368–382

    Google Scholar 

  • NMSM Techow C O’Ryan (2004) ArticleTitleCharacterization of microsatellite loci in white-chinned petrel (Procellaria aequinoctialis) and cross-amplification in six other Procellariiform species Mol. Ecol. Notes 4 33–35 Occurrence Handle10.1046/j.1471-8286.2003.00560.x Occurrence Handle1:CAS:528:DC%2BD2cXitlymu7g%3D

    Article  CAS  Google Scholar 

  • AR Templeton RJ Robertson J Brisson J Strasburg (2001) ArticleTitleDisrupting evolutionary processes: the effect of habitat fragmentation on collared lizards in the Mizzouri Ozarks Proc. Natl. Acad. Sci. USA 98 5426–5432 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wgtbc%3D Occurrence Handle11344289

    CAS  PubMed  Google Scholar 

  • RJ Tomkins (1985) ArticleTitleBreeding success and mortality of dark-rumped petrels in the Galápagos, and control of their predators ICBP Tech. Publ. 3 159–175

    Google Scholar 

  • RJ Tomkins BJ Milne (1991) ArticleTitleDifferences among dark-rumped petrel (Pterodroma phaeopygia) populations within the Galápagos Archipelago Notornis 38 1–35

    Google Scholar 

  • A Tye HL Snell SB Peck H Adsersen (2002) Outstanding terrestrial features of the Galápagos archipelago R Bensted-Smith (Eds) A Biodiversity Vision for the Galápagos Islands Charles Darwin Foundation and World Wildlife Fund Puerto Ayora, Galápagos 12–23

    Google Scholar 

  • J Warham (1990) The petrels: their ecology and breeding systems Academic Press New York

    Google Scholar 

  • GA Wilson B Rannala (2003) ArticleTitleBayesian inference of recent migration rates using multilocus genotypes Genetics 163 1177–1191 Occurrence Handle12663554

    PubMed  Google Scholar 

  • S Wright (1931) ArticleTitleEvolution in Mendelian populations Genetics 16 97–159

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Queen’s University, Kingston, Ontario, K7L 3N6, Canada

    Vicki L. Friesen

  2. Agencia Española de Cooperación Internacional – Programa Araucaria, Francisco Salazar E12-73 y Toledo, Quito, Ecuador

    José A. González

  3. Parque Nacional Galápagos, Oficina Técnica San Cristóbal, Galápagos, Ecuador

    Francisco Cruz-Delgado

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  1. Vicki L. Friesen
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  2. José A. González
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  3. Francisco Cruz-Delgado
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Correspondence to Vicki L. Friesen.

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Friesen, V.L., González, J.A. & Cruz-Delgado, F. Population Genetic Structure and Conservation of the Galápagos Petrel (Pterodroma phaeopygia). Conserv Genet 7, 105–115 (2006). https://doi.org/10.1007/s10592-005-8704-6

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